Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics
International audience Recent studies revealed that several vibrio species have evolved the capacity to survive inside host cells. However, it is still often ignored if intracellular stages are required for pathogenicity. Virulence of Vibrio tasmaniensis LGP32, a strain pathogenic for Crassostrea gi...
Published in: | Environmental Microbiology |
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Main Authors: | , , , , , , , , , , , , , |
Other Authors: | , , , , , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
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HAL CCSD
2016
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Subjects: | |
Online Access: | https://doi.org/10.1111/1462-2920.13083 https://hal-sde.archives-ouvertes.fr/hal-01311061/file/Vanhove-2016-EnvMicrobiol-Copper-MANUSCRIT.pdf https://hal-sde.archives-ouvertes.fr/hal-01311061 |
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language |
English |
topic |
envir socio |
spellingShingle |
envir socio Vanhove, A.S. Rubio, T.P. Nguyen, A.N. Lemire, A. Roche, D. Nicod, J. Vergnes, Agnès Poirier, Aurore Disconzi, E. Bachère, Evelyne Le Roux, F. Jacq, Annick Charrière, Guillaume M Destoumieux-Garzón, Delphine Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics |
topic_facet |
envir socio |
description |
International audience Recent studies revealed that several vibrio species have evolved the capacity to survive inside host cells. However, it is still often ignored if intracellular stages are required for pathogenicity. Virulence of Vibrio tasmaniensis LGP32, a strain pathogenic for Crassostrea gigas oysters, depends on entry into hemocytes, the oyster immune cells. We investigated here the mechanisms of LGP32 intracellular survival and their consequences on the host-pathogen interaction. Entry and survival inside hemocytes were required for LGP32-driven cytolysis of hemocytes, both in vivo and in vitro. LGP32 intracellular stages showed a profound boost in metabolic activity and a major transcription of antioxidant and copper detoxification genes, as revealed by RNA sequencing. LGP32 isogenic mutants showed that resistance to oxidative stress and copper efflux are two main functions required for vibrio intracellular stages and cytotoxicity to hemocytes. Copper efflux was also essential for host colonization and virulence in vivo. Altogether our results identify copper resistance as a major mechanism to resist killing by phagocytes, induce cytolysis of immune cells and colonize oysters. Selection of such resistance traits could arise from vibrio interactions with copper-rich environmental niches including marine invertebrates, which favor the emergence of pathogenic vibrios resistant to intraphagosomal killing across animal species. |
author2 |
Interactions Hôtes-Pathogènes-Environnements (IHPE) Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Perpignan Via Domitia (UPVD) Institut de Biologie Intégrative de la Cellule (I2BC) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS) Signalisation et Réseaux de Régulations Bactériens (SRRB) Département Biologie des Génomes (DBG) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS) Laboratoire de Biologie Intégrative des Modèles Marins (LBI2M) Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Station biologique de Roscoff Roscoff (SBR) Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Génomique métabolique (UMR 8030) Genoscope - Centre national de séquençage Evry (GENOSCOPE) Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE) |
format |
Article in Journal/Newspaper |
author |
Vanhove, A.S. Rubio, T.P. Nguyen, A.N. Lemire, A. Roche, D. Nicod, J. Vergnes, Agnès Poirier, Aurore Disconzi, E. Bachère, Evelyne Le Roux, F. Jacq, Annick Charrière, Guillaume M Destoumieux-Garzón, Delphine |
author_facet |
Vanhove, A.S. Rubio, T.P. Nguyen, A.N. Lemire, A. Roche, D. Nicod, J. Vergnes, Agnès Poirier, Aurore Disconzi, E. Bachère, Evelyne Le Roux, F. Jacq, Annick Charrière, Guillaume M Destoumieux-Garzón, Delphine |
author_sort |
Vanhove, A.S. |
title |
Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics |
title_short |
Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics |
title_full |
Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics |
title_fullStr |
Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics |
title_full_unstemmed |
Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics |
title_sort |
copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics |
publisher |
HAL CCSD |
publishDate |
2016 |
url |
https://doi.org/10.1111/1462-2920.13083 https://hal-sde.archives-ouvertes.fr/hal-01311061/file/Vanhove-2016-EnvMicrobiol-Copper-MANUSCRIT.pdf https://hal-sde.archives-ouvertes.fr/hal-01311061 |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_source |
Hyper Article en Ligne - Sciences de l'Homme et de la Société ISSN: 1462-2912 EISSN: 1462-2920 Environmental Microbiology Environmental Microbiology, Society for Applied Microbiology and Wiley-Blackwell, 2016, Pathogen Ecology, 18 (3), pp.875-888. ⟨10.1111/1462-2920.13083⟩ |
op_relation |
hal-01311061 doi:10.1111/1462-2920.13083 10670/1.hs8xo5 https://hal-sde.archives-ouvertes.fr/hal-01311061/file/Vanhove-2016-EnvMicrobiol-Copper-MANUSCRIT.pdf https://hal-sde.archives-ouvertes.fr/hal-01311061 |
op_rights |
other |
op_doi |
https://doi.org/10.1111/1462-2920.13083 |
container_title |
Environmental Microbiology |
container_volume |
18 |
container_issue |
3 |
container_start_page |
875 |
op_container_end_page |
888 |
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1766394500024893440 |
spelling |
fttriple:oai:gotriple.eu:10670/1.hs8xo5 2023-05-15T15:58:44+02:00 Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics Vanhove, A.S. Rubio, T.P. Nguyen, A.N. Lemire, A. Roche, D. Nicod, J. Vergnes, Agnès Poirier, Aurore Disconzi, E. Bachère, Evelyne Le Roux, F. Jacq, Annick Charrière, Guillaume M Destoumieux-Garzón, Delphine Interactions Hôtes-Pathogènes-Environnements (IHPE) Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Perpignan Via Domitia (UPVD) Institut de Biologie Intégrative de la Cellule (I2BC) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS) Signalisation et Réseaux de Régulations Bactériens (SRRB) Département Biologie des Génomes (DBG) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Intégrative de la Cellule (I2BC) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS) Laboratoire de Biologie Intégrative des Modèles Marins (LBI2M) Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Station biologique de Roscoff Roscoff (SBR) Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Génomique métabolique (UMR 8030) Genoscope - Centre national de séquençage Evry (GENOSCOPE) Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE) 2016-01-01 https://doi.org/10.1111/1462-2920.13083 https://hal-sde.archives-ouvertes.fr/hal-01311061/file/Vanhove-2016-EnvMicrobiol-Copper-MANUSCRIT.pdf https://hal-sde.archives-ouvertes.fr/hal-01311061 en eng HAL CCSD Society for Applied Microbiology and Wiley-Blackwell hal-01311061 doi:10.1111/1462-2920.13083 10670/1.hs8xo5 https://hal-sde.archives-ouvertes.fr/hal-01311061/file/Vanhove-2016-EnvMicrobiol-Copper-MANUSCRIT.pdf https://hal-sde.archives-ouvertes.fr/hal-01311061 other Hyper Article en Ligne - Sciences de l'Homme et de la Société ISSN: 1462-2912 EISSN: 1462-2920 Environmental Microbiology Environmental Microbiology, Society for Applied Microbiology and Wiley-Blackwell, 2016, Pathogen Ecology, 18 (3), pp.875-888. ⟨10.1111/1462-2920.13083⟩ envir socio Journal Article https://vocabularies.coar-repositories.org/resource_types/c_6501/ 2016 fttriple https://doi.org/10.1111/1462-2920.13083 2023-01-22T18:29:24Z International audience Recent studies revealed that several vibrio species have evolved the capacity to survive inside host cells. However, it is still often ignored if intracellular stages are required for pathogenicity. Virulence of Vibrio tasmaniensis LGP32, a strain pathogenic for Crassostrea gigas oysters, depends on entry into hemocytes, the oyster immune cells. We investigated here the mechanisms of LGP32 intracellular survival and their consequences on the host-pathogen interaction. Entry and survival inside hemocytes were required for LGP32-driven cytolysis of hemocytes, both in vivo and in vitro. LGP32 intracellular stages showed a profound boost in metabolic activity and a major transcription of antioxidant and copper detoxification genes, as revealed by RNA sequencing. LGP32 isogenic mutants showed that resistance to oxidative stress and copper efflux are two main functions required for vibrio intracellular stages and cytotoxicity to hemocytes. Copper efflux was also essential for host colonization and virulence in vivo. Altogether our results identify copper resistance as a major mechanism to resist killing by phagocytes, induce cytolysis of immune cells and colonize oysters. Selection of such resistance traits could arise from vibrio interactions with copper-rich environmental niches including marine invertebrates, which favor the emergence of pathogenic vibrios resistant to intraphagosomal killing across animal species. Article in Journal/Newspaper Crassostrea gigas Unknown Environmental Microbiology 18 3 875 888 |